The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes

ABSTRACT Various intracellular bacterial symbionts that provide their host with essential nutrients have much-reduced genomes, attributed largely to genomic decay and relaxed selection. To obtain quantitative estimates of the metabolic function of these bacteria, we reconstructed genome- and transcr...

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Autores principales:	Nana Y. D. Ankrah, Bessem Chouaia, Angela E. Douglas
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2018
Materias:	constraint-based modeling flux balance analysis nitrogen recycling symbiosis xylem-feeding insects Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/239240cb01fd40e6850ccdefc58672e3
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spelling	oai:doaj.org-article:239240cb01fd40e6850ccdefc58672e32021-11-15T15:58:20ZThe Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes10.1128/mBio.01433-182150-7511https://doaj.org/article/239240cb01fd40e6850ccdefc58672e32018-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01433-18https://doaj.org/toc/2150-7511ABSTRACT Various intracellular bacterial symbionts that provide their host with essential nutrients have much-reduced genomes, attributed largely to genomic decay and relaxed selection. To obtain quantitative estimates of the metabolic function of these bacteria, we reconstructed genome- and transcriptome-informed metabolic models of three xylem-feeding insects that bear two bacterial symbionts with complementary metabolic functions: a primary symbiont, Sulcia, that has codiversified with the insects, and a coprimary symbiont of distinct taxonomic origin and with different degrees of genome reduction in each insect species (Hodgkinia in a cicada, Baumannia in a sharpshooter, and Sodalis in a spittlebug). Our simulations reveal extensive bidirectional flux of multiple metabolites between each symbiont and the host, but near-complete metabolic segregation (i.e., near absence of metabolic cross-feeding) between the two symbionts, a likely mode of host control over symbiont metabolism. Genome reduction of the symbionts is associated with an increased number of host metabolic inputs to the symbiont and also reduced metabolic cost to the host. In particular, Sulcia and Hodgkinia with genomes of ≤0.3 Mb are calculated to recycle ∼30 to 80% of host-derived nitrogen to essential amino acids returned to the host, while Baumannia and Sodalis with genomes of ≥0.6 Mb recycle 10 to 15% of host nitrogen. We hypothesize that genome reduction of symbionts may be driven by selection for increased host control and reduced host costs, as well as by the stochastic process of genomic decay and relaxed selection. IMPORTANCE Current understanding of many animal-microbial symbioses involving unculturable bacterial symbionts with much-reduced genomes derives almost entirely from nonquantitative inferences from genome data. To overcome this limitation, we reconstructed multipartner metabolic models that quantify both the metabolic fluxes within and between three xylem-feeding insects and their bacterial symbionts. This revealed near-complete metabolic segregation between cooccurring bacterial symbionts, despite extensive metabolite exchange between each symbiont and the host, suggestive of strict host controls over the metabolism of its symbionts. We extended the model analysis to investigate metabolic costs. The positive relationship between symbiont genome size and the metabolic cost incurred by the host points to fitness benefits to the host of bearing symbionts with small genomes. The multicompartment metabolic models developed here can be applied to other symbioses that are not readily tractable to experimental approaches.Nana Y. D. AnkrahBessem ChouaiaAngela E. DouglasAmerican Society for Microbiologyarticleconstraint-based modelingflux balance analysisnitrogen recyclingsymbiosisxylem-feeding insectsMicrobiologyQR1-502ENmBio, Vol 9, Iss 5 (2018)
institution	DOAJ
collection	DOAJ
language	EN
topic	constraint-based modeling flux balance analysis nitrogen recycling symbiosis xylem-feeding insects Microbiology QR1-502
spellingShingle	constraint-based modeling flux balance analysis nitrogen recycling symbiosis xylem-feeding insects Microbiology QR1-502 Nana Y. D. Ankrah Bessem Chouaia Angela E. Douglas The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes
description	ABSTRACT Various intracellular bacterial symbionts that provide their host with essential nutrients have much-reduced genomes, attributed largely to genomic decay and relaxed selection. To obtain quantitative estimates of the metabolic function of these bacteria, we reconstructed genome- and transcriptome-informed metabolic models of three xylem-feeding insects that bear two bacterial symbionts with complementary metabolic functions: a primary symbiont, Sulcia, that has codiversified with the insects, and a coprimary symbiont of distinct taxonomic origin and with different degrees of genome reduction in each insect species (Hodgkinia in a cicada, Baumannia in a sharpshooter, and Sodalis in a spittlebug). Our simulations reveal extensive bidirectional flux of multiple metabolites between each symbiont and the host, but near-complete metabolic segregation (i.e., near absence of metabolic cross-feeding) between the two symbionts, a likely mode of host control over symbiont metabolism. Genome reduction of the symbionts is associated with an increased number of host metabolic inputs to the symbiont and also reduced metabolic cost to the host. In particular, Sulcia and Hodgkinia with genomes of ≤0.3 Mb are calculated to recycle ∼30 to 80% of host-derived nitrogen to essential amino acids returned to the host, while Baumannia and Sodalis with genomes of ≥0.6 Mb recycle 10 to 15% of host nitrogen. We hypothesize that genome reduction of symbionts may be driven by selection for increased host control and reduced host costs, as well as by the stochastic process of genomic decay and relaxed selection. IMPORTANCE Current understanding of many animal-microbial symbioses involving unculturable bacterial symbionts with much-reduced genomes derives almost entirely from nonquantitative inferences from genome data. To overcome this limitation, we reconstructed multipartner metabolic models that quantify both the metabolic fluxes within and between three xylem-feeding insects and their bacterial symbionts. This revealed near-complete metabolic segregation between cooccurring bacterial symbionts, despite extensive metabolite exchange between each symbiont and the host, suggestive of strict host controls over the metabolism of its symbionts. We extended the model analysis to investigate metabolic costs. The positive relationship between symbiont genome size and the metabolic cost incurred by the host points to fitness benefits to the host of bearing symbionts with small genomes. The multicompartment metabolic models developed here can be applied to other symbioses that are not readily tractable to experimental approaches.
format	article
author	Nana Y. D. Ankrah Bessem Chouaia Angela E. Douglas
author_facet	Nana Y. D. Ankrah Bessem Chouaia Angela E. Douglas
author_sort	Nana Y. D. Ankrah
title	The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes
title_short	The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes
title_full	The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes
title_fullStr	The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes
title_full_unstemmed	The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes
title_sort	cost of metabolic interactions in symbioses between insects and bacteria with reduced genomes
publisher	American Society for Microbiology
publishDate	2018
url	https://doaj.org/article/239240cb01fd40e6850ccdefc58672e3
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The Cost of Metabolic Interactions in Symbioses between Insects and Bacteria with Reduced Genomes

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